Fisheries Faculty, Istanbul University, Ordu Cad. No. 200, Laleli, Fatih-Istanbul, Turkey. 3

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1 ACTA ZOOLOGICA BULGARICA Acta zool. bulg., 65 (2), 2013: Microhabitat Distribution of Pseudodactylogyrus anguillae (Monogenea), Ergasilus gibbus and Ergasilus lizae (Copepoda) on the Gills of European Eels (Anguilla anguilla, L.) Erhan Soylu 1 *, Sibel Özesen Çolak 2, Fatime Erdogan 3, Mete Erdogan 3, Necla Tektas 1 1 Fisheries Department, Vocational School of Technical Sciences, Marmara University, Göztepe, Kadıköy-Istanbul, Turkey. 2 Fisheries Faculty, Istanbul University, Ordu Cad. No. 200, Laleli, Fatih-Istanbul, Turkey. 3 Aquaculture Programme, Ortaca Vocational School, Muğla University, Ortaca, Muğla, Turkey. Abstract: Microhabitat distribution of Pseudodactylogyrus anguillae (Yin & Sproston, 1948) Gussev, 1965 (Monogenea: Dactylogyridae), Ergasilus gibbus von Nordman, 1832 and Ergasilus lizae Kroyer, 1863 (Copepoda: Ergasilidae) was studied on the gills of European eel Anguilla anguilla from Lake Köyceğiz-Dalyan, Estuarine Channel System, Turkey. A total of 69 A. anguilla were examined between December 2009 and March A total of 1421 P. anguillae, 143 E. gibbus and 63 E. lizae specimens were collected from the fish host. A prevalence of 81.15% and mean infection intensity of for P. anguillae, 50.72%, 4.0 for E. gibbus and 27.53%, 3.31 for E. lizae were found. Gill arches II, III, IV were preferred by P. anguillae, gill arches I, II, III by E. gibbus and gill arches III, IV by E. lizae. In general occurrence of the parasite species, P. anguillae preferred proximal-dorsal segments, E. gibbus distal-dorsal segments, whereas E. lizae exhibited a rather homogenous distribution. Site of attachment was the inner surface of the gill arches for E. gibbus and the outer surface for E. lizae. P. anguillae was found mostly on the inner surface of the hemibranches. Bispecific infections of P. anguillae with E. gibbus and E. lizae were also analysed individually. Finally, single species infections of the three parasite species were analysed. Key words: gill parasite, microhabitat, Monogenea, Copepoda, fish host, ectoparasites. Introduction The monogenean gill parasites P. anguillae and P. bini are known to occur on the gills of the Asian eel Anguilla japonica and the Australian eel Anguilla reinharditi. P. bini was first reported in 1929 by Kikuchi in Japan and P. bini and P. anguillae were reported in 1948 by Yin & Sproston 1948 in China. P. anguillae and P. bini are rather pathogenic to Anguilla spp. and can cause mortality in heavily infected fish (Ge l n a r et al. 1996). Both these monogeneans were apparently introduced via the Japanese eel A. japonica and were first reported in Anguilla anguilla in the Soviet Union (Go l o v i n 1977). They have been reported on the gills of both wild and cultured eels from Hungary (Mo l n a r 1984), France (La m b e rt et al. 1985), Italy (Sa r o g l i a et al. 1985), Denmark (Bu c h m a n n et al. 1987) and Poland (Dz i k a et al. 1995). Co n e, Ma r c o g l i e s e (1995) were the first to record P. anguillae on the gills of the American eel Anguilla rostrata in North America. A. anguilla is an economically valuable fish species in Turkey. However it is not farmed, all harvesting is done by fishing. The number of studies on the parasites of A. anguilla in Turkey is limited; Alt u n e l (1990) investigated the parasite fauna in A. anguilla in the Ekinli Lagoon, Ge n ç et al. (2005) studied the occurrence of the swimbladder parasite Anguillicola crassus in the same fish host in the Ceyhan River. * Corresponding author: * Correspondence author: Tel: Fax: esoylu@marmara.edu.tr 251

2 Soylu E., S. Özesen Ç., F. Erdogan, M. Erdogan, N. Tektas The coexistence of gill monogeneans has been studied widely (El-Ha f İdİ 1998, Dz i k a 1989, Ko s k i va a et al. 1991, Si m k o va et al. 2000, Tu r g u t et al. 2006). Numerous studies have investigated the spatial distribution and microhabitats selection of the monogenean gill parasites of Anguilla anguilla (Bu c h m a n n 1989; Ro d r i g u e s, Sa r a i va 1996, Dz i k a 1999, Mat e j u s o va et al. 2003). However, only a few studies have investigated co-occurrent copepods and monogeneans (Ramasamy et al. 1985, Ba k e r, Co n e 2000, Baker et al. 2005). The present study investigated the microhabitat distribution of the monogenean Pseudodactylogyrus anguillae in co-occurrence with the copepods Ergasilus gibbus and Ergasilus lizae on the gills of the European eel Anguilla anguilla. Materials and Methods Fig. 1. Map of the study area. The Köyceğiz-Dalyan Nature Reserve is an important wetland area in South-western Turkey (36 45 and N, and E). The outflow of Lake Köyceğiz, the Dalyan River enlarges into a labyrinth-like channel system, discharging into the Mediterranean Sea (Fig. 1). The estuarine area includes three lakes (Alagöl, Sülüngür and Sülüklü). The Dalyan channel system is fed by Lake Köyceğiz. The Mediterranean Sea has many sulphuric thermal springs located both on the bottom and around it. The Köyceğiz-Dalyan estuarine channel system is 14 km in length and connects the meromictic Lake Köyceğiz and the Mediterranean Sea. The Dalyan water mass consists of a mixohaline upper layer from Lake Köyceğiz and a lower layer of the Mediterranean Sea saline water mixed with the sulphuric thermal spring water (Ka z a n c i et al. 2003). A total of 69 Anguilla anguilla of mean (± sd) total length 52.5 ±10.24 cm (range cm) and mean (± sd) weight ± g (range g) were examined between December 2009 and March Fish were caught by local fishermen and transferred alive to the laboratory in aerated lake water. After each eel was sacrificed all branchial arches from the left and the right sides were removed and placed in 4% formalin solution for further studies. Each gill arch was placed in a separate Petri dish filled with water, when examined. The gill arches were numbered I to IV from anterior to posterior. Each arch was divided into three gill segments: dorsal, medial and ventral; two gill areas: proximal and distal; two gill surfaces: outer and inner; two gill hemibranches: anterior and posterior, as a niche for parasites (Fig. 2). All monogenean and copepod parasites on the gills were collected one by one from each sector separately under a stereomicroscope at 20X magnification and the exact location of the parasites was recorded before removal. The monogenean parasites were cleared in glycerine or lactophenol and identified on the basis of their chitinous elements according to Pu g a c h e v et al. (2010). Copepod parasites were roughly sorted into two groups on the basis of their second antenna, and preserved in 70% ethanol for further identification on the basis of the keys of Ba u e r (1987). Kruskal-Wallis tests were used to test the significance of the differences in the number of parasites between the dorsal, medial and ventral segments. The differences in the parasite numbers between the proximal and distal parts, left and right sides, and gill arches were tested using the Mann Whitney U-test. Differences of P < 0.05 were considered significant. Results A total of 69 Anguilla anguilla were examined, 4 of which (5.8%) were not infected at all, 56 (81%) 252

3 Microhabitat Distribution of Pseudodactylogyrus anguillae (Monogenea), Ergasilus gibbus and... were infected by Pseudodactylogyrus anguillae, 34 (49%) by Ergasilus gibbus and 19 (28%) by E. lizae. In only 5 of the infected fish were there simultaneous infections of E. gibbus and E. lizae with P. anguillae. A total of 1421 P. anguillae, 143 E. gibbus and 63 E. lizae individuals were recorded in general occurrence. The overall prevalence, mean intensity and mean abundance for P. anguillae were found to be 81.2%, 25.4, 20.6, for E. gibbus 49.3%, 4.2, 2.1 and for E. lizae 27.5%, 3.3, 0.9 respectively. The infection intensities (per eel) of P. anguillae, E. gibbus and E. lizae respectively ranged between 1-202, 1-41 and 1-14 individuals. Fig. 2. Division of branchial arch (1-2-3 Distal part, Proximal part). General occurrence of the parasites Branchial distribution of P. anguillae, E. gibbus and E. lizae on the gills of Anguilla anguilla was examined. Of the 69 dissected fish, 56 were infected with Pseudodactylogyrus anguillae (prevalence 81.2%). The distribution of 1421 P. anguillae in general occurrence is shown (Table 1). The differences were not found to be significant between the number of P. anguillae on the left and right gill arches (P=0.861 > 0.05). Gill arches II, III and IV were preferred over I. The differences were significant between the numbers of P. anguillae found on the segments (P=0.00 < 0.05), P. anguillae preferred dorsal segments (84.1%), namely 55.9% of the P. anguillae settled in sector 4 and then 28.2% in sector 3. There were no statistically significant differences in the number of the parasites between the proximal and distal parts (P=0.225 > 0.05), 64.9% of P. anguillae were recorded on the proximal part, 80.0% of P. anguillae preferred the inner surface, 52.6% settled in the anterior hemibraches. Of the 69 examined fish, 34 were infected with Ergasilus gibbus (prevalence 49.3%). A total of 143 E. gibbus were recorded. E. gibbus did not show preference for the left or right side of the gill (P Table 1. General occurrence of Pseudodactylogyrus anguillae, Ergasilus gibbus and Ergasilus lizae on the gills of Anguilla anguilla. P. anguillae E. gibbus E. lizae Number of infected eels Mean intensity Number % Number % Number % Left side Right side Gill arch I Gill arch II Gill arch III Gill arch IV Dorsal segment Medial segment Ventral segment Proximal part Distal part Anterior hemibranch Posterior hemibranch Inner surface Outer surface

4 Soylu E., S. Özesen Ç., F. Erdogan, M. Erdogan, N. Tektas =0.341 > 0.05), E. gibbus preferred gill arches I, II and III. A significantly greater number of E. gibbus occurred on the dorsal segment of the gills (65.7%) than on the medial and ventral segments (P=0.00 < 0.05). E. gibbus preferred distal part of the gill arches (79.7%) and significant differences were found with the proximal part (P=0.001 < 0.05). E. gibbus did not show preference for anterior or posterior hemibranches, and 95.1% of the parasites occupied the inner surface of the gill hemibranches. Of the 69 examined fish, 19 were infected with Ergasilus lizae (prevalence 27.5%). A total of 63 E. lizae were recorded. E. lizae did not show preference for the left or right side of the gills (P=0.283 > 0.05), gill arches IV and III were preferably infected, differences between the number of E. lizae on gill arches IV-III and I-II were found to be significant (P=0.00 < 0.05). But distribution of E. lizae both on dorsal, medial, ventral segments and proximal, distal parts was found rather homogenous. E. lizae preferred outer surface (95.2%) of the hemibranches. E. lizae did not show preference for anterior or posterior hemibranches and the left or right side. Bispecific infections Bispecific infections of A. anguilla were examined with P. anguillae E. gibbus and P. anguillae E. lizae combinations. Of the 69 eels examined, 24 were infected with only P. anguillae E. gibbus (prevalence 34.8%). In these eels, 849 P. anguillae and 133 E. gibbus were recorded. P. anguillae preferred gill arches II, III and IV, dorsal segments (86.0%), and proximal part (60.7%). E. gibbus preferred gill arches I and II, dorsal segments (64.7%), distal part (77.4%) and inner surface (94.0%) of the hemibranches (Table 2). Of the 69 eels examined, 10 were infected with only P. anguillae E. lizae (prevalence 14.5%). In these eels, 175 P. anguillae and 44 E. lizae were recorded. P. anguillae did not show a right or left side preference. P. anguillae preferred gill arches II and III, dorsal segment (84.0%), proximal part (71.4%) and inner surface (88.6%). In these bispecific infections, E. lizae preferred the left side (prevalence 61.4%). E. lizae preferred gill arches IV and III, dorsal (40.9%) and medial (36.4%) segments. E. lizae were evenly distributed over both proximal and distal parts, and they all (100%) were found on the outer surface of the hemibranches (Table 2). Monospecific infections A total of 17 eels (prevalence 24.6%) were infected with only P. anguillae, 5 eels (7.2%) with only E. gibbus and 4 eels (5.8%) with only E. lizae. A total of 397 P. anguillae were recorded in these monospecific infections. P. anguillae settled in gill arches II, III and IV more frequently. The species predominantly occurred on dorsal segments (79.1%), significant differences were found between Table 2. Distribution of Pseudodactylogyrus anguillae Ergasilus gibbus and Pseudodactylogyrus anguillae Ergasilus lizae on the gills of Anguilla anguilla in bispecific infections. 254 P. anguillae E. gibbus P. anguillae E.lizae Number of infected eels Mean intensity Number % Number % Number % Number % Left side Right side Gill arch I Gill arch II Gill arch III Gill arch IV Dorsal segment Medial segment Ventral segment Proximal part Distal part Anterior hemibranch Posterior hemibranch Inner surface Outer surface

5 Microhabitat Distribution of Pseudodactylogyrus anguillae (Monogenea), Ergasilus gibbus and... the numbers recorded on the dorsal and the other two segments (P=0.00 < 0.05). Although there were no statistically significant differences in the number of P. anguillae between proximal and distal parts (P=0.195 > 0.05), the parasite preferred proximal parts (72.0%), inner surface of the hemibranches (75.8%), but no differences were found between the left and right side (P=0.975 > 0.05). A total of 10 E. gibbus were recorded in these monospecific infections. E. gibbus preferred gill arch I (40.0%) and no parasite was found on arch IV. Dorsal segments were mainly preferred by E. gibbus (70.0%), the parasite completely occupied the distal part (100%), inner surface (100%), and it was mainly found on the right side (70.0%). Dorsal segments mainly preferred by E. gibbus (70.0%), parasite totally occupied distal part (100%), inner surface (100%) and of the (70.0%) found on the right side. A total of 11 E. lizae were recorded in these monospecific infections. E. lizae preferred gill arch IV, with no parasite being found on gill arch I. E. lizae mostly preferred medial segments (63.6%). There were no significant differences in the number of E. lizae between the proximal and distal parts (P=0.949 > 0.05), but the parasite exhibited preference for the left side (P=0.027 < 0.05); 81.8% of the E. lizae found were on the left side and 90.9% were on the outer surface of the hemibranches (Table 3). The numbers of P. anguillae, E. gibbus and E. lizae between bispecific and monospecific infections were also examined. The numbers of P. anguillae showed no statistically significant difference between bispecific infections with E. gibbus, bispecific infections with E. lizae and monospecific infections (Kruskal-Wallis test P=0.404; p > 0.05). There was no statistically significant difference in the numbers of E. gibbus between bispecific infections with P. anguillae and monospecific infections (Mann-Whitney U test P=359 > 0.05). There were no statistically significant differences in the numbers of E. lizae between bispecific infections with P. anguillae and monospecific infections (Mann-Whitney U test P=0.663 > 0.05). Table 3. Distribution of Pseudodactylogyrus anguillae, Ergasilus gibbus and Ergasilus lizae on the gills of Anguilla anguilla in monospecific infections. P. anguillae E. gibbus E. lizae Number of infected eels Mean intensity Number % Number % Number % Left side Right side Gill arch I Gill arch II Gill arch III Gill arch IV Dorsal segment Medial segment Ventral segment Proximal part Distal part Anterior hemibranch Posterior hemibranch Inner surface Outer surface Table 4. Number of Pseudodactylogyrus anguillae, Ergasilus gibbus and E. lizae according to fish size. Total length (cm) P. anguillae E. gibbus E. lizae Number % Number % Number %

6 Soylu E., S. Özesen Ç., F. Erdogan, M. Erdogan, N. Tektas P. anguillae, E. gibbus and E. lizae were recorded in simultaneous infections in only 5 fish hosts but were not taken into account because of the low sample size. The prevalence and the number of P. anguillae increased with the size of the host and reached 45.2% and 643 individuals in the 55.0 cm and higher size classes. The highest prevalence of E. gibbus 50.3% and 72 individuals was found in the cm size classes. The highest prevalence of E. lizae 76.2% and 48 individuals was found in the 55.0 cm and higher size classes (Table 4). Discussion Statistical analysis showed that P. anguillae preferred the dorsal segments; this preference was observed in the general occurrence of the three parasites, in P. anguillae E. gibbus and P. anguillae E. lizae bispecific infections and moreover in monospecific infections. P. anguillae significantly preferred dorsal segments, proximal halves and inner surfaces of the hemibranches in general occurrence, bispecific and monospecific infections. According to Bu c h m a n n (1988), P. anguillae which has large hamuli, are never found embedded in a tissue reaction and thus they preferably attach more to intact gills and the more sheltered base of gill filaments. In contrast, P. bini attach more effectively to gills, as it appears that the filaments are ones with small hamuli, and it prefers distal parts (Bu c h m a n n 1987). Ll e w e l ly n (1956) and Suydam (1971) both stated that parasite distribution over the arches is highly affected by respiratory current flow rate distribution. The greatest volume of water in the gill ventilation current pass over the second and third gill arches (Pa l i n g 1968). The dorsal segments, proximal halves and inner surface of the primary filaments of each hemibranch are more sheltered than the outer parts (Wo o t t e n 1974). The findings mentioned above, evidence the microhabitat preference of P. anguillae. In the present study, the significant preference for arches II, III, and IV over arch I, dorsal segments, proximal halves, inner surface of the hemibranches and no preference for the left or right side was observed for P. anguillae. Prevalence and mean intensity of P. anguillae were higher when it coexisted with E. gibbus in bispecific infections. In general occurrence and bispecific infections, E. gibbus had no significant left or right side preference, but in monospecific infections E. gibbus preferred the right side. E. gibbus preferred gill arches I, II and III in general occurrence, and arches I and II in bispecific infections with P. anguillae. All E. gibbus were found on the inner surfaces of the hemibranches except for 4.9% on the outer surface in general occurrence. There were no significant differences of E. lizae on the left or right side of the branchial apparatus in general occurrence and bispecific infections with P. anguillae, but E. lizae preferred the left side in monospecific infections, however these findings are most likely a reflection of a smaller sample size, like the right side preference of E. gibbus in monospecific infection. But on the other hand, E. lizae did also show left side preference in bispecific infections with P. anguillae. E. lizae preferred gill arches III and IV, dorsal medial and ventral segments in general occurrence and in bispecific infections, but in monospecific infections E. lizae was found in arch IV, and the medial segment. In all infections, E. lizae were recorded on both proximal and distal segments, strongly preferring the outer surfaces of the hemibranches and not being found at all on the inner surface. In conclusion, our data indicate that the distribution of P. anguillae over the gill arches was not random. Even when numbers of P. anguillae were high, vacant niches were clear, and the parasite showed significant preference for the dorsal segment to the median and ventral segments. This aggregation of P. anguillae on the dorsal segments suggests the absence of intraspecific competition. From the parasite distribution observed on the gills of A. anguilla, it showed that niches of P. anguillae and E. gibbus overlapped each other and that there was no interspecific competition. E. gibbus preferred anterior, E. lizae posterior gill arches. E. gibbus preferred inner, E. lizae outer surface and E. gibbus preferred arch I, E. lizae arch IV. Besides these, a record of E. gibbus and E. lizae coexisting with P. anguillae in simultaneous infections in only 5 eels indicate negative interactions between them. Acknowledgements: We sincerely thank Dr. Hoda El Rashidy for confirmation of copepod specimens as Ergasilus lizae and the Dalyan Fisheries Cooperative (Muğla-Köyceğiz) for providing fish specimens. 256

7 References Microhabitat Distribution of Pseudodactylogyrus anguillae (Monogenea), Ergasilus gibbus and... Alt u n e l F. N Investigation on parasite fauna of eels (Anguilla Anguilla) in Ekinli Lagoon. Prof thesis. University of Uludag, Turkey, 55 p. Baker T. G., E. Pante, I. Buron Co-occurence of Naobranchia lizae (Copepoda) and Metamicrocotyla macracantha (Monogenea), gill parasites of the striped mullet Mugil cephalus. Parasitology Research, 97: Ba r k e r D. E., D. K. Co n e Occurrence of Ergasilus celestis (Copepoda) and Pseudodactylogyrus anguillae (Monogenea) among wild eels (Anguilla rostrata) in relation to stream flow, ph and temperature and recommendations for controlling their transmission among captive eels. Aquaculture, 187: Ba u e r O. N Key for parasite determination of freshwater fish fauna USSR. In: Volume I3, Academy of Sciences USSR. Published by Nauka, Leningrad. (In Russian). BUCHMANN K., S. MELLERGAARD, M. KOIE Pseudodactylogyrus infections in eels: review. 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